Laser‐ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia
Abstract
Summary Technologies enabling in situ metabolic profiling of living plant systems are invaluable for understanding physiological processes and could be used for rapid phenotypic screening (e.g., to produce plants with superior biological nitrogen‐fixing ability). The symbiotic interaction between legumes and nitrogen‐fixing soil bacteria results in a specialized plant organ (i.e., root nodule) where the exchange of nutrients between host and endosymbiont occurs. Laser‐ablation electrospray ionization mass spectrometry ( LAESI ‐ MS ) is a method that can be performed under ambient conditions requiring minimal sample preparation. Here, we employed LAESI ‐ MS to explore the well characterized symbiosis between soybean ( Glycine max L. Merr.) and its compatible symbiont, Bradyrhizobium japonicum . The utilization of ion mobility separation ( IMS ) improved the molecular coverage, selectivity, and identification of the detected biomolecules. Specifically, incorporation of IMS resulted in an increase of 153 differentially abundant spectral features in the nodule samples. The data presented demonstrate the advantages of using LAESI – IMS – MS for the rapid analysis of intact root nodules, uninfected root segments, and free‐living rhizobia. Untargeted pathway analysis revealed several metabolic processes within the nodule (e.g., zeatin, riboflavin, and purine synthesis). Compounds specific to the uninfected root and bacteriamore »
- Authors:
-
[3]
- Department of Chemistry W. M. Keck Institute for Proteomics Technology and Applications The George Washington University Washington DC 20052 USA
- Divisions of Plant Sciences and Biochemistry C. S. Bond Life Sciences Center University of Missouri Columbia MO 65211 USA
- Environmental Molecular Sciences Laboratory Earth and Biological Sciences Directorate Pacific Northwest National Laboratory 902 Battelle Boulevard Richland WA 99354 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1401532
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Name: The Plant Journal Journal Volume: 91 Journal Issue: 2; Journal ID: ISSN 0960-7412
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Stopka, Sylwia A., Agtuca, Beverly J., Koppenaal, David W., Paša‐Tolić, Ljiljana, Stacey, Gary, Vertes, Akos, and Anderton, Christopher R. Laser‐ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia. United Kingdom: N. p., 2017.
Web. doi:10.1111/tpj.13569.
Stopka, Sylwia A., Agtuca, Beverly J., Koppenaal, David W., Paša‐Tolić, Ljiljana, Stacey, Gary, Vertes, Akos, & Anderton, Christopher R. Laser‐ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia. United Kingdom. https://doi.org/10.1111/tpj.13569
Stopka, Sylwia A., Agtuca, Beverly J., Koppenaal, David W., Paša‐Tolić, Ljiljana, Stacey, Gary, Vertes, Akos, and Anderton, Christopher R. Tue .
"Laser‐ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia". United Kingdom. https://doi.org/10.1111/tpj.13569.
@article{osti_1401532,
title = {Laser‐ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia},
author = {Stopka, Sylwia A. and Agtuca, Beverly J. and Koppenaal, David W. and Paša‐Tolić, Ljiljana and Stacey, Gary and Vertes, Akos and Anderton, Christopher R.},
abstractNote = {Summary Technologies enabling in situ metabolic profiling of living plant systems are invaluable for understanding physiological processes and could be used for rapid phenotypic screening (e.g., to produce plants with superior biological nitrogen‐fixing ability). The symbiotic interaction between legumes and nitrogen‐fixing soil bacteria results in a specialized plant organ (i.e., root nodule) where the exchange of nutrients between host and endosymbiont occurs. Laser‐ablation electrospray ionization mass spectrometry ( LAESI ‐ MS ) is a method that can be performed under ambient conditions requiring minimal sample preparation. Here, we employed LAESI ‐ MS to explore the well characterized symbiosis between soybean ( Glycine max L. Merr.) and its compatible symbiont, Bradyrhizobium japonicum . The utilization of ion mobility separation ( IMS ) improved the molecular coverage, selectivity, and identification of the detected biomolecules. Specifically, incorporation of IMS resulted in an increase of 153 differentially abundant spectral features in the nodule samples. The data presented demonstrate the advantages of using LAESI – IMS – MS for the rapid analysis of intact root nodules, uninfected root segments, and free‐living rhizobia. Untargeted pathway analysis revealed several metabolic processes within the nodule (e.g., zeatin, riboflavin, and purine synthesis). Compounds specific to the uninfected root and bacteria were also detected. Lastly, we performed depth profiling of intact nodules to reveal the location of metabolites to the cortex and inside the infected region, and lateral profiling of sectioned nodules confirmed these molecular distributions. Our results established the feasibility of LAESI – IMS – MS for the analysis and spatial mapping of plant tissues, with its specific demonstration to improve our understanding of the soybean‐rhizobial symbiosis.},
doi = {10.1111/tpj.13569},
journal = {The Plant Journal},
number = 2,
volume = 91,
place = {United Kingdom},
year = {Tue May 23 00:00:00 EDT 2017},
month = {Tue May 23 00:00:00 EDT 2017}
}
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Works referenced in this record:
Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement
journal, March 2006
- Schauer, Nicolas; Semel, Yaniv; Roessner, Ute
- Nature Biotechnology, Vol. 24, Issue 4
21 Tesla Fourier Transform Ion Cyclotron Resonance Mass Spectrometer Greatly Expands Mass Spectrometry Toolbox
journal, October 2016
- Shaw, Jared B.; Lin, Tzu-Yung; Leach, Franklin E.
- Journal of The American Society for Mass Spectrometry, Vol. 27, Issue 12
Purine Biosynthesis. Big in Cell Division, Even Bigger in Nitrogen Assimilation
journal, March 2002
- Smith, Penelope M. C.; Atkins, Craig A.
- Plant Physiology, Vol. 128, Issue 3
Ion Mobility Spectrometry: Principles and Applications
journal, August 2006
- Borsdorf, Helko; Eiceman, Gary A.
- Applied Spectroscopy Reviews, Vol. 41, Issue 4
Metabolic characterization of tomato fruit during preharvest development, ripening, and postharvest shelf-life
journal, October 2011
- Oms-Oliu, Gemma; Hertog, M. L. A. T. M.; Van de Poel, B.
- Postharvest Biology and Technology, Vol. 62, Issue 1
In vivo energetics and control of nitrogen fixation: changes in the adenylate energy charge and adenosine 5'-diphosphate/adenosine 5'-triphosphate ratio of cells during growth on dinitrogen versus growth on ammonia.
journal, January 1980
- Upchurch, R. G.; Mortenson, L. E.
- Journal of Bacteriology, Vol. 143, Issue 1
A purple acid phosphatase plays a role in nodule formation and nitrogen fixation in Astragalus sinicus
journal, June 2015
- Wang, Jianyun; Si, Zaiyong; Li, Fang
- Plant Molecular Biology, Vol. 88, Issue 6
Saponin and sapogenol. XLII. Structures of acetyl-soyasaponins A1, A2, and A3, astringent partially acetylated bisdesmosides of soyasapogenol A, from american soybean, the seeds of Glycine max MERRILL.
journal, January 1988
- Kitagawa, Isao; Taniyama, Toshio; Nagahama, Yoshiko
- CHEMICAL & PHARMACEUTICAL BULLETIN, Vol. 36, Issue 8
Bioactive Molecules in Soil Ecosystems: Masters of the Underground
journal, April 2013
- Zhuang, Xuliang; Gao, Jie; Ma, Anzhou
- International Journal of Molecular Sciences, Vol. 14, Issue 5
Metabolite profiling of mycorrhizal roots of Medicago truncatula
journal, January 2008
- Schliemann, Willibald; Ammer, Christian; Strack, Dieter
- Phytochemistry, Vol. 69, Issue 1
Variations in the Abundance of Lipid Biomarker Ions in Mass Spectrometry Images Correlate to Tissue Density
journal, November 2016
- Bilkey, Jade; Tata, Alessandra; McKee, Trevor D.
- Analytical Chemistry, Vol. 88, Issue 24
The Rhizobium-plant symbiosis
journal, March 1995
- van Rhijn, P.; Vanderleyden, J.
- Microbiological Reviews, Vol. 59, Issue 1
Saponins, classification and occurrence in the plant kingdom
journal, February 2007
- Vincken, Jean-Paul; Heng, Lynn; de Groot, Aede
- Phytochemistry, Vol. 68, Issue 3
Systems Biology Update: Cell Type-Specific Transcriptional Regulatory Networks
journal, December 2009
- Pu, Li; Brady, Siobhan
- Plant Physiology, Vol. 152, Issue 2
Genetics and functional genomics of legume nodulation
journal, April 2006
- Stacey, Gary; Libault, Marc; Brechenmacher, Laurent
- Current Opinion in Plant Biology, Vol. 9, Issue 2
Study of adenosine 5′-mono-, di- and triphosphates in plant tissues. IV. Regulation of the level of nucleotides, in vivo, by adenylate kinase: Theoretical and experimental study
journal, August 1968
- Bomsel, Jean-Loup; Pradet, Alain
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 162, Issue 2
Genomics-based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula: Biosynthesis of saponins
journal, February 2005
- Achnine, Lahoucine; Huhman, David V.; Farag, Mohamed A.
- The Plant Journal, Vol. 41, Issue 6
Ion mobility-mass spectrometry strategies for untargeted systems, synthetic, and chemical biology
journal, February 2015
- May, Jody C.; Goodwin, Cody R.; McLean, John A.
- Current Opinion in Biotechnology, Vol. 31
Ion Suppression in Mass Spectrometry
journal, July 2003
- Annesley, T. M.
- Clinical Chemistry, Vol. 49, Issue 7
Molecular basis of symbiosis between Rhizobium and legumes
journal, May 1997
- Freiberg, Christoph; Fellay, Rémy; Bairoch, Amos
- Nature, Vol. 387, Issue 6631
Sinorhizobium meliloti Flavin Secretion and Bacteria-Host Interaction: Role of the Bifunctional RibBA Protein
journal, May 2014
- Yurgel, Svetlana N.; Rice, Jennifer; Domreis, Elizabeth
- Molecular Plant-Microbe Interactions, Vol. 27, Issue 5
Studies on Nitrogen-Fixing Blue-Green Algae. I. Growth and Nitrogen Fixation by Anabaena Cylindrica Lemm
journal, July 1955
- Allen, M. B.; Arnon, Daniel I.
- Plant Physiology, Vol. 30, Issue 4
Pyrimidine and Purine Biosynthesis and Degradation in Plants
journal, June 2006
- Zrenner, Rita; Stitt, Mark; Sonnewald, Uwe
- Annual Review of Plant Biology, Vol. 57, Issue 1
Plant Sugar-Response Pathways. Part of a Complex Regulatory Web
journal, December 2000
- Gibson, Susan I.
- Plant Physiology, Vol. 124, Issue 4
Investigating carbohydrate isomers by IMS-CID-IMS-MS: precursor and fragment ion cross-sections
journal, January 2015
- Gaye, M. M.; Kurulugama, R.; Clemmer, D. E.
- The Analyst, Vol. 140, Issue 20
MALDI mass spectrometry-assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula - Sinorhizobium meliloti symbiosis
journal, May 2013
- Ye, Hui; Gemperline, Erin; Venkateshwaran, Muthusubramanian
- The Plant Journal, Vol. 75, Issue 1
Ion Mobility Derived Collision Cross Sections to Support Metabolomics Applications
journal, March 2014
- Paglia, Giuseppe; Williams, Jonathan P.; Menikarachchi, Lochana
- Analytical Chemistry, Vol. 86, Issue 8
B IOSYNTHESIS OF V ITAMIN B 2 (R IBOFLAVIN )
journal, July 2000
- Bacher, A.; Eberhardt, S.; Fischer, M.
- Annual Review of Nutrition, Vol. 20, Issue 1
Laser Ablation Electrospray Ionization for Atmospheric Pressure, in Vivo, and Imaging Mass Spectrometry
journal, November 2007
- Nemes, Peter; Vertes, Akos
- Analytical Chemistry, Vol. 79, Issue 21
Fundamentals of Traveling Wave Ion Mobility Spectrometry
journal, December 2008
- Shvartsburg, Alexandre A.; Smith, Richard D.
- Analytical Chemistry, Vol. 80, Issue 24, p. 9689-9699
Heme Synthesis in Soybean Root Nodules: I. On the Role of Bacteroid δ-Aminolevulinic Acid Synthase and δ-Aminolevulinic Acid Dehydrase in the Synthesis of the Heme of Leghemoglobin
journal, September 1977
- Nadler, Kenneth D.; Avissar, Yeal J.
- Plant Physiology, Vol. 60, Issue 3
Investigation of triterpene synthesis and regulation in oats reveals a role for -amyrin in determining root epidermal cell patterning
journal, May 2014
- Kemen, A. C.; Honkanen, S.; Melton, R. E.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 23
Nutrient Sharing between Symbionts
journal, June 2007
- White, James; Prell, Jurgen; James, Euan K.
- Plant Physiology, Vol. 144, Issue 2
Ambient molecular imaging by laser ablation electrospray ionization mass spectrometry with ion mobility separation
journal, February 2015
- Li, Hang; Smith, Brian K.; Márk, László
- International Journal of Mass Spectrometry, Vol. 377
A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis
journal, January 2007
- Murray, J. D.; Karas, B. J.; Sato, S.
- Science, Vol. 315, Issue 5808
Requirement for Riboflavin for Effective Symbiosis on Clover by an Auxotrophic Mutant Strain of Rhizobium Trifolii
journal, January 1970
- Schwinghamer, Ea
- Australian Journal of Biological Sciences, Vol. 23, Issue 5
An overview of the metabolic differences between Bradyrhizobium japonicum 110 bacteria and differentiated bacteroids from soybean ( Glycine max ) root nodules: an in vitro 13 C- and 31 P-nuclear magnetic resonance spectroscopy study
journal, March 2013
- Vauclare, Pierre; Bligny, Richard; Gout, Elisabeth
- FEMS Microbiology Letters, Vol. 343, Issue 1
Metabolomic Profiling of Bradyrhizobium diazoefficiens-Induced Root Nodules Reveals Both Host Plant-Specific and Developmental Signatures
journal, May 2016
- Lardi, Martina; Murset, Valérie; Fischer, Hans-Martin
- International Journal of Molecular Sciences, Vol. 17, Issue 6
Multifaceted Investigation of Metabolites During Nitrogen Fixation in Medicago via High Resolution MALDI-MS Imaging and ESI-MS
journal, October 2014
- Gemperline, Erin; Jayaraman, Dhileepkumar; Maeda, Junko
- Journal of The American Society for Mass Spectrometry, Vol. 26, Issue 1
Top-down mass spectrometry imaging of intact proteins by laser ablation ESI FT-ICR MS
journal, February 2014
- Kiss, András; Smith, Donald F.; Reschke, Brent R.
- PROTEOMICS, Vol. 14, Issue 10
Mass Spectrometry in Plant-omics
journal, March 2016
- Gemperline, Erin; Keller, Caitlin; Li, Lingjun
- Analytical Chemistry, Vol. 88, Issue 7
Metabolic transformation of microalgae due to light acclimation and genetic modifications followed by laser ablation electrospray ionization mass spectrometry with ion mobility separation
journal, January 2014
- Stopka, Sylwia A.; Shrestha, Bindesh; Maréchal, Éric
- The Analyst, Vol. 139, Issue 22
Mass spectrometric analysis of lipo-chitin oligosaccharides-Signal molecules mediating the host-specific legume-rhizobium symbiosis
journal, January 1998
- van der Drift, Koen M. G. M.; Olsthoorn, Maurien M. A.; Brüll, Lars P.
- Mass Spectrometry Reviews, Vol. 17, Issue 2
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms
journal, June 2006
- Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G.
- Annual Review of Plant Biology, Vol. 57, Issue 1
Does GABA increase the efficiency of symbiotic N 2 fixation in legumes?
journal, January 2011
- Sulieman, Saad
- Plant Signaling & Behavior, Vol. 6, Issue 1
Resolving Structural Isomers of Monosaccharide Methyl Glycosides Using Drift Tube and Traveling Wave Ion Mobility Mass Spectrometry
journal, March 2012
- Li, Hongli; Giles, Kevin; Bendiak, Brad
- Analytical Chemistry, Vol. 84, Issue 7
mMass data miner: an open source alternative for mass spectrometric data analysis
journal, January 2008
- Strohalm, Martin; Hassman, Martin; Košata, Bedřich
- Rapid Communications in Mass Spectrometry, Vol. 22, Issue 6
GC–MS based metabolite profiling implies three interdependent ways of ammonium assimilation in Medicago truncatula root nodules
journal, December 2006
- Barsch, Aiko; Carvalho, Helena G.; Cullimore, Julie V.
- Journal of Biotechnology, Vol. 127, Issue 1
Profiling of primary metabolite by means of capillary electrophoresis-mass spectrometry and its application for plant science
journal, January 2009
- Harada, Kazuo; Fukusaki, Eiichiro
- Plant Biotechnology, Vol. 26, Issue 1
Products of Biological Nitrogen Fixation in Higher Plants: Synthesis, Transport, and Metabolism
journal, June 1986
- Schubert, K. R.
- Annual Review of Plant Physiology, Vol. 37, Issue 1
Rhizobium-Legume Symbiosis and Nitrogen Fixation under Severe Conditions and in an Arid Climate
journal, December 1999
- Zahran, Hamdi Hussein
- Microbiology and Molecular Biology Reviews, Vol. 63, Issue 4
Biological activities and distribution of plant saponins
journal, October 2004
- Sparg, S. G.; Light, M. E.; van Staden, J.
- Journal of Ethnopharmacology, Vol. 94, Issue 2-3
Metabolomics – the link between genotypes and phenotypes
journal, January 2002
- Fiehn, Oliver
- Plant Molecular Biology, Vol. 48, Issue 1/2, p. 155-171
The effect of inoculating endophytic N2-fixing bacteria on micropropagated sugarcane plants
journal, May 2002
- Oliveira, A. L. M.; Urquiaga, S.; Döbereiner, J.
- Plant and Soil , Vol. 242, 205-215
Early signaling, synthesis, transport and metabolism of ureides
journal, April 2016
- Baral, Bikash; Teixeira da Silva, Jaime A.; Izaguirre-Mayoral, Maria Luisa
- Journal of Plant Physiology, Vol. 193
Roles for Riboflavin in the Sinorhizobium -Alfalfa Association
journal, May 2002
- Yang, Guoping; Bhuvaneswari, T. V.; Joseph, Cecillia M.
- Molecular Plant-Microbe Interactions, Vol. 15, Issue 5
M ETABOLOMICS IN S YSTEMS B IOLOGY
journal, June 2003
- Weckwerth, Wolfram
- Annual Review of Plant Biology, Vol. 54, Issue 1
Mass spectrometry-based metabolomics
journal, January 2006
- Dettmer, Katja; Aronov, Pavel A.; Hammock, Bruce D.
- Mass Spectrometry Reviews, Vol. 26, Issue 1
Global reprogramming of transcription and metabolism in M edicago truncatula during progressive drought and after rewatering : Drought-stressed
journal, May 2014
- Zhang, Ji-Yi; Cruz De Carvalho, Maria H.; Torres-Jerez, Ivone
- Plant, Cell & Environment, Vol. 37, Issue 11
Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus
journal, August 2004
- Colebatch, Gillian; Desbrosses, Guilhem; Ott, Thomas
- The Plant Journal, Vol. 39, Issue 4
Ion Mobility Analysis of Molecular Dynamics
journal, April 2014
- Wyttenbach, Thomas; Pierson, Nicholas A.; Clemmer, David E.
- Annual Review of Physical Chemistry, Vol. 65, Issue 1
Localization of Fatty Acyl and Double Bond Positions in Phosphatidylcholines Using a Dual Stage CID Fragmentation Coupled with Ion Mobility Mass Spectrometry
journal, June 2011
- Castro-Perez, Jose; Roddy, Thomas P.; Nibbering, Nico M. M.
- Journal of The American Society for Mass Spectrometry, Vol. 22, Issue 9
Internal energy deposition and ion fragmentation in atmospheric-pressure mid-infrared laser ablation electrospray ionization
journal, January 2012
- Nemes, Peter; Huang, Hehua; Vertes, Akos
- Physical Chemistry Chemical Physics, Vol. 14, Issue 7
Spatially-resolved plant metabolomics: some potentials and limitations of Laser-Ablation Electrospray Ionization (LAESI) Mass Spectrometry metabolite imaging
journal, September 2015
- Etalo, Desalegn; de Vos, Ric CH; Joosten, Matthieu H. A. J.
- Plant Physiology
Metabolite profiling for plant functional genomics
journal, November 2000
- Fiehn, Oliver; Kopka, Joachim; Dörmann, Peter
- Nature Biotechnology, Vol. 18, Issue 11
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI)
journal, September 2007
- Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave
- Metabolomics, Vol. 3, Issue 3
Metabolic Diversification--Independent Assembly of Operon-Like Gene Clusters in Different Plants
journal, April 2008
- Field, B.; Osbourn, A. E.
- Science, Vol. 320, Issue 5875
The Galactolipid Digalactosyldiacylglycerol Accumulates in the Peribacteroid Membrane of Nitrogen-fixing Nodules of Soybean and Lotus
journal, May 2004
- Gaude, Nicole; Tippmann, Helge; Flemetakis, Emmanouil
- Journal of Biological Chemistry, Vol. 279, Issue 33
Direct Plant Tissue Analysis and Imprint Imaging by Desorption Electrospray Ionization Mass Spectrometry
journal, July 2011
- Müller, Thomas; Oradu, Sheran; Ifa, Demian R.
- Analytical Chemistry, Vol. 83, Issue 14
Metabolite profiling and assessment of metabolome compartmentation of soybean leaves using non-aqueous fractionation and GC-MS analysis
journal, August 2007
- Benkeblia, Noureddine; Shinano, Takuro; Osaki, Mitsuru
- Metabolomics, Vol. 3, Issue 3
High-Throughput Cell and Tissue Analysis with Enhanced Molecular Coverage by Laser Ablation Electrospray Ionization Mass Spectrometry Using Ion Mobility Separation
journal, April 2014
- Shrestha, Bindesh; Vertes, Akos
- Analytical Chemistry, Vol. 86, Issue 9
Complete Transcriptome of the Soybean Root Hair Cell, a Single-Cell Model, and Its Alteration in Response to Bradyrhizobium japonicum Infection
journal, November 2009
- Libault, Marc; Farmer, Andrew; Brechenmacher, Laurent
- Plant Physiology, Vol. 152, Issue 2
Turnover rates in microorganisms by laser ablation electrospray ionization mass spectrometry and pulse-chase analysis
journal, January 2016
- Stopka, Sylwia A.; Mansour, Tarek R.; Shrestha, Bindesh
- Analytica Chimica Acta, Vol. 902
Distinct, crucial roles of flavonoids during legume nodulation
journal, July 2007
- Subramanian, Senthil; Stacey, Gary; Yu, Oliver
- Trends in Plant Science, Vol. 12, Issue 7
Development of the Legume Root Nodule
journal, November 1991
- Brewin, Nicholas J.
- Annual Review of Cell Biology, Vol. 7, Issue 1
Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes
journal, June 2008
- Oldroyd, Giles E. D.; Downie, J. Allan
- Annual Review of Plant Biology, Vol. 59, Issue 1
Metabolome Analysis of Arabidopsis thaliana Roots Identifies a Key Metabolic Pathway for Iron Acquisition
journal, July 2014
- Schmidt, Holger; Günther, Carmen; Weber, Michael
- PLoS ONE, Vol. 9, Issue 7
Ion mobility-mass spectrometry
journal, January 2008
- Kanu, Abu B.; Dwivedi, Prabha; Tam, Maggie
- Journal of Mass Spectrometry, Vol. 43, Issue 1
Two interconnected B vitamins: riboflavin and pyridoxine
journal, October 1989
- McCormick, D. B.
- Physiological Reviews, Vol. 69, Issue 4
Triterpene Biosynthesis in Plants
journal, April 2014
- Thimmappa, Ramesha; Geisler, Katrin; Louveau, Thomas
- Annual Review of Plant Biology, Vol. 65, Issue 1